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Kudoa Ogawai (Myxosporea: Kudoidae) Infection in Cultured Olive Flounder Paralichthys Olivaceus

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Kudoa Ogawai (Myxosporea: Kudoidae) Infection in Cultured Olive Flounder Paralichthys Olivaceus ISSN (Print) 0023-4001 ISSN (Online) 1738-0006 Korean J Parasitol Vol. 57, No. 4: 439-444, August 2019 ▣ BRIEF COMMUNICATION https://doi.org/10.3347/kjp.2019.57.4.439 Kudoa ogawai (Myxosporea: Kudoidae) Infection in Cultured Olive Flounder Paralichthys olivaceus 1,2 1,2 1,2 1,2, Sang Phil Shin , Chang Nam Jin , Han Chang Sohn , Jehee Lee * 1Department of Marine Life Science, Jeju National University, Jeju Self-Governing Province 63243, Korea; 2Fish Vaccine Research Center, Jeju National University, Jeju Self-Governing Province 63243, Korea Abstract: Since Kudoa septempuntata was identified as a causative agent of food poisoning associated with raw olive flounder Paralichthys olivaceus, interest and concern regarding the parasite have increased. However, there have been no investigations or reports of other Kudoa species infecting the fish (except for K. paralichthys, which infects the brain) in Korea. We found cysts filled with myxospores of Kudoa species in muscles of cultured olive flounder specimens and identified these to the species level. Mature spores were quadrate, measuring 8.7± 0.5 µm in length, 9.2± 0.4 µm in thick- ness, and 12.9± 0.6 µm in width. The spores containing 4 polar capsules had a length of 2.1± 0.2 µm and a width of 1.8± 0.3 µm. The partial 18S and 28S rDNA of isolates showed 99-100% similarities with K. ogawai. Using these morpho- logical and molecular analyses, the species was identified as K. ogawai. This study is the first report of K. ogawai infection in cultured olive flounder in Korea. Key words: Kudoa ogawai, olive flounder, identification, foodborne disease Myxozoans are parasites that complete a life cycle through flounder cultured in Jeju island and has isolated another Ku- vertebrate (mainly fish) and invertebrate (mainly annelid) doa sp. from olive flounder muscle. The aim of the present hosts [1]. The genus Kudoa contains myxosporeans with 4 or study was to identify the Kudoa sp. using morphological and more shall valves and polar capsules, and the parasites infect molecular analyses and to reveal differences between the pres- various fish species [2,3]. Some Kudoa spp. reduce the com- ent isolate and other Kudoa spp. known to infect olive floun- mercial value of fish by causing post-mortem liquefaction der. In addition, the information obtained from this study will (such as K. thyrsites, K. lateolabracis, and K. neothunni) [3-7], be applied to the inspection and identification of Kudoa spp. cyst formation in muscles (K. iwatai and K. amamiensis) [8,9], Olive flounder samples (n=2, 56.4±4.3 cm) were obtained and spinal deformation (K. yasunagai) [2,10,11]. In addition, from an olive flounder farm situated on Jeju island. The fish previous studies have reported the relationship between Kudoa samples were examined microscopically to detect K. septem- spp. and food-poisoning [12-14]. These findings have led to punctata spores in squash preparations, and cysts filled with increased interest and concern regarding Kudoa infection in another Kudoa sp. were found. The cysts were collected using commercially important fish. Olive flounder, Paralichthys oliva- forceps and were squashed on a glass slide. The spores were ceus, is an important fish species cultured in Korea, and there wet mounted and observed under a light microscope and pho- have been several reports of myxosporean infections (Entero- tographed at 400×or 1,000×magnification. Measurements of myxum leei, Parvicapsula anisocaudata, P. curvatura, and Sinuolin- myxospores were obtain from 20 spores using the ImageJ im- ea capsularis), including Kudoa spp. (K. septempunctata and K. age processing software (available at http://rsb.info.nih.gov/ paralichthys), in the fish [15-19]. The Fish Vaccine Research ij/) according to Lom and Arthur’s criteria (1989) [20]. Center has been monitoring the parasitic infections of olive The myxospores were collected and passed through a 40 µm cell strainer. DNA was extracted from partially purified para- Received 8 May 2019, revised 30 July 2019, accepted 31 July 2019. sites using the AccuPrep Genomic DNA Extraction Kit (Bi- • Corresponding author ([email protected]) * oneer, Daejeon, Korea) following the manufacturer’s instruc- © 2019, Korean Society for Parasitology and Tropical Medicine tions. Portions of 18S and 28S rDNA were amplified by PCR This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) using a combination of primers that we (28S-KO2000F: 5′ which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. -CTGTCCGTACCGAATCCG-3′) and other groups (18S-18e: 5′ 439 440 Korean J Parasitol Vol. 57, No. 4: 439-444, August 2019 -CTGGTTGATCCTGCCAGT-3′, 18S-MyxospecF: 5′-TTCT- myxospores were quadrate in the apical view and had 4 equal GCCCTATCAACTWGTTG-3′, 18S-MyxospecR: 5′-GGTTTCN spore valves, each containing one polar capsule with a round- CDGRGGGMCCAAC-3′, 18S-ERIB10: 5′-CTTCCGCAG- ed peripheral edge. In addition, the appearance of the 4 polar GTTCACCTA-3′, 28S-Kt28SF: 5′-CAAGACTACCTGCTGAAC-3′, capsules was similar to a 4-leaf clover (Fig. 1D). In side view, 28S-NLF1050: 5′-AATCGAACCATCTAGTAGCTGG-3′, 28S- spores were rounded triangle-shaped, and prominent apical NLR1270: 5′-TTCATCCCGCATCGCCAGTTC-3′, 28S- projections were observed (Fig. 1E). The spores measured NLR1694(mo): 5′-GTTAGGCAATGGCTTAGGACC-3′, 28S-3R: 8.7±0.5 µm (8.3-9.6 µm) in length, 9.2±0.4 µm (8.4-10.0 5′-GAGCACTGGGCAGAAATC-3′, 28S-NLR3113(mo): 5′-GTC- µm) in thickness, and 12.9±0.6 µm (11.5-13.9 µm) in width. TAAACCCAGCTCACGTTC-3′, and 28S-NLR3284: 5′-TTCT- The polar capsule length was 2.1 ±0.2 µm (1.7-2.5 μm) and GACTTAGAGGCGTTCAG-3′) have designed [2,16,21-25]. PCR polar capsule width was 1.8±0.3 µm (1.4-2.5 µm) (Table 1). products were treated with the AccuPrep Genomic PCR Purifi- The species isolated in the present study was then compared cation Kit (Bioneer) to remove excess primers and dNTPs, and with 8 Kudoa spp. that have been previously reported in olive were directly sequenced using BigDyeTM Terminator v3.1 in flounder. Kudoa ogawai was the most similar to the isolated an ABI 3730xl Sequencer. The 18S and 28S rDNA sequences species in terms of measurements and shape of spores, num- of isolates were compared in the GenBank database using the ber of valves per spore, apical projection, and infection site. Basic Local Alignment Search Tool (BLAST) search engine to Kudoa paralichthys and K. shiomitsui showed similarities to the find sequences with a high degree of similarity. Multiple align- isolate in terms of spore shape and number of valves per ments of 18S rDNA sequences were made using Clustal X 2.0 spore. However, they are smaller than the isolate and have a [26] with 7 homologous sequences from Kudoa spp. and one different infection site (brain and heart vs muscle). In addi- sequence from E. leei (outgroup) reported in olive flounder tion, they have small projections that are not easily observed, (except K. lateolabracis). The phylogenetic tree was constructed while the isolate has distinct apical projections. Although K. using the neighbor-joining method in MEGA 7 [27]. lateolabracis and K. thyrsites had similarities number of valves Oval cysts 1 mm in length approximately, were observed in per spore and share the same infection site as the isolate, they the squashed muscle sample (Fig. 1A). Cysts were shorter in have distinct spore shapes with one large polar capsule. Kudoa length and thicker than the pseudocysts of K. septempunctata septempunctata and K. igami have similar spore measurements that are usually detected, and the myxospores were also differ- and the same infection site as the isolate. However, they have a ent in form from those of K. septempunctata (Fig. 1B, C). The different spore shape (stellate vs. quadrate) as well as a differ- A B C Fig. 1. Kudoa ogawai found in the muscle of Paralichthys olivaceus. (A) Cyst and (B) myxospores of K. ogawai. Scale bar= 100 and 20 µm, respectively. (C) Myxospores of K. septempunctata. Scale bar= 20 µm. (D) Fresh spores of K. ogawai in apical view and (E) side view. Arrows and arrowheads show the polar capsule and the apical pro- jections of spores, respectively. Scale D E bar= 10 µm. Table 1. Comparison of Kudoa sp. (present isolate) with the other Kudoa spp. reported in olive flounders Paralichthys olivaceus Spore Spore Spore Polar capsule Polar capsule Spore shape Apical Infection Species References length thickness width length width (Np. of valves per spore) projections site Kudoa sp. 8.7± 0.5 9.2± 0.4 12.9± 0.6 2.1± 0.2 1.8± 0.3 Quadrate (4) + Muscle Present (8.3-9.6) (8.4-10.0) (11.5-13.9) (1.7-2.5) (1.4-2.5) study K. ogawai 9.5± 0.5 9.9± 0.7 12.3± 0.7 - - Quadrate (4) + Muscle [28] K. septempunctata 7.9-8.9 8.9-10.0 11.1-13.1 3.7-5.3 2.2-2.8 Stellate (6/7) Tiny projections Muscle [29] K. lateolabracisa 5.4-6.9 9.9-12.9 8.4-9.9 (Max) 4.0-5.9 (Large) 2.5-3.5 (Large) Quadrate with unequal - Muscle [4] 5.9-6.9 (Min) 3.0-4.0 (Small) 1.5-2.0 (Small) polar capsule (4) K. thyrsites 6.9-8.9 12.9-17.8 7.9-11.9 (Max) 4.0-5.9 (Large) 1.5-3.0 (Large) Quadrate with unequal - Muscle [4] 6.9-7.9 (Min) 2.0-4.0 (Large) 1.5-2.5 Large) polar capsule (4) K.
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